Impact of intermittent fasting (5:2) on ketone body production in healthy female subjects - ernährungs umschau
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Impact of intermittent fasting (5:2)
on ketone body production in healthy
female subjects
Christin Cerniuc+, Tobias Fischer+, Anna Baumeister, Ursula Bordewick-Dell
Introduction
Abstract
Intermittent fasting is a growing trend – used for weight loss and for in- One of the greatest health policy challenges we
creasing well-being. This nutrition strategy consists of fasting for short pe- currently face is the “obesity epidemic”. Obe-
riods over the course of a day, or over the course of a whole week. During sity is associated with various metabolic com-
longer fasting periods, the main ketone body beta-hydroxybutyrate (βHB) plications such as insulin resistance, dyslipi-
plays an important role in energy supply. The 5:2 diet consists of eating demia, hypertension, type 2 diabetes mellitus,
normally on 5 days of the week and fasting for 2 non-consecutive days. and cardiovascular disease, all of which can
In this single-arm, non-controlled, interventional study, 19 healthy female be countered through weight loss. Accord-
subjects followed the 5:2 diet over a 7-day interventional period. 13 of the ing to current recommendations, this can be
subjects completed the study. achieved through moderate restriction of daily
Through the measurement of blood ketone (βHB) levels, it was demons- energy intake [1].
trated that there was a marked increase in ketone body levels in the blood In recent years, there has been increasing dis-
during the aforementioned fasting period. During the second fasting day, cussion around periodic energy restriction in
adaptation was already observable. There was a reduction in βHB values
the form of intermittent fasting (IF) as an al-
and an increase in blood glucose concentration, together with a simul-
ternative nutrition strategy for weight man-
taneous reduction in the occurrence of unfavorable effects such as dizzi-
ness, shaking, tachycardia, and nausea. agement and management of metabolic dys-
functions [2–9]. Intermittent fasting involves
Keywords: intermittent fasting, ketone bodies, beta-hydroxybutyrate,
a period of fasting that is repeated at regular
weight loss, prevention, energy restriction
intervals over the course of a certain amount
of time – a day or a week [1].
In the case of time-restricted feeding (TRF),
food intake is restricted to a defined time
window during the day [10]. Here, the natural
break from eating that occurs during sleep at
night creates an overnight fasting (OF) period.
Extending the OF period achieves the require-
ments for TRF [11].
The most well-known TRF method is the 16:8
method, in which the fasting period is 16 out
of 24 hours, and eating is restricted to a period
of 8 hours [10]. Alternate-day fasting (ADF) is
fasting on every second day. Therefore, in the
case of ADF, one day of fasting is immediately
Citation followed by one day of normal, unrestricted
Cerniuc C, Fischer T, Baumeister A, Bordewick-Dell U (2019) food intake. In the 5:2 method of IF, food in-
Impact of intermittent fasting (5:2) on ketone body production
take is normal for five days of the week, and
in healthy female subjects. Ernahrungs Umschau 66(1): 2–9
energy intake is drastically restricted on the
This article is available online:
DOI: 10.4455/eu.2019.002 remaining two days of the week (fasting) [10].
These diets were made famous through book
Peer-reviewed
Manuscript (Original) received: 11.06.2018
Revision accepted: 19.07.2018 +
The authors contributed equally to this paper.
2 Ernaehrungs Umschau international | 1/2019
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Reproduction and dissemination – also partial – applicable to all media only
with written permission of Umschau Zeitschriftenverlag GmbH, Wiesbaden.
publications for the general market starting from the year 2013. the study (calculated drop-out rate = 32%).
The 5:2 Diet was made famous by Mosley (“The Fast Diet”), ADF The subjects selected for the study were fema-
was made famous by Varady (“The Every Other Day Diet”), and les with an average age of 21.5 ± 2.5 years,
“The 2-day Diet” was made famous by Harvie [12–14]. BMI 21.6 ± 1.6 kg/m². The reasons for study
drop-out were time constraints (n = 3) or
The positive metabolic changes that occur in IF are attributed to acute illness prior to the start of the inter-
the metabolic switch from mainly carbohydrate metabolism to vention (n = 2). One subject discontinued her
mainly fat metabolism. Mobilization of free fatty acids from the study participation on the first day of fasting
adipose tissue increases. These fatty acids are partly used to form due to feeling unwell (n = 1).
ketone bodies through ketogenesis. The ketone bodies can in turn
be used directly by certain organs and can also be used by the Ethical considerations
brain as an alternative energy substrate instead of glucose after a Prior to initiation of the study, the study
period of adaptation. was reviewed by the Ethics Committee of the
Beta-hydroxybutyrate (βHB) is one of the main ketone bodies in- Westphalia-Lippe Medical Association and the
volved in energy supply [15, 16]. Since ketogenesis takes effect Westphalian Wilhelm University [Ethikkom-
after only a short period of abstention from food, it is possible mission der Ärztekammer Westfalen-Lippe and of
that the formation of ketone bodies also has a decisive impact on Westfälische Wilhelms-Universität] (2017-245-
the positive effects of IF that have been demonstrated in studies. f-S). Checks were carried out to ensure that
There is mounting evidence that βHB not only supplies energy, there was no dependent relationship between
but also performs signaling functions, both on the cell surface the subjects and the study staff. The subjects
and inside the cell, which affect factors such as gene expression, were only included in the study after being
fat metabolism, neuronal function, and metabolic rate [17, 18]. informed in detail about the study and after
These molecular signaling functions could have an impact on a giving their written consent to participation
range of human diseases such as type 2 diabetes mellitus and (informed consent). During the study, there
Alzheimer’s dementia. were no deviations from the study protocol
that was submitted to the Ethics Committee.
In order to better understand the metabolic situation in humans
during short-term abstention from food, an interventional nu- Study design and study conduct
tritional study was carried out to investigate the effect of IF on The subjects in this single-arm interventional
ketogenesis, using the 5:2 method as an example. The short-term study without a control group were instruct-
change in βHB concentration in the capillary blood on repeated ed in how to carry out intermittent fasting
fasting days with complete energy restriction was chosen as the according to the 5:2 method during the week
primary endpoint because this has not yet been investigated in of intervention. Prior to the start of the in-
studies on IF using the 5:2 Diet [3–6, 19–22]. tervention, and after the subjects had been
informed about how the study will be con-
ducted and had signed the informed consent
form, they were instructed in detail about the
Methodology fasting method, including with regard to the
devices that were to be used to measure the ca-
Study subjects pillary blood parameters (βHB, glucose). Body
The study subjects (healthy subjects) were recruited through weight was measured on the information day
posters and through direct announcements in lecture halls at the and after the entire intervention was complete,
Münster University of Applied Sciences. Positive responses were and height was measured once.
followed up with an online screening questionnaire to check eligi- In accordance with the requirements of in-
bility according to the inclusion and exclusion criteria. termittent fasting, normal food intake was
The inclusion criteria were age between 18 and 30 years, BMI required for 5 days of the week, and com-
within the normal range (18–25 kg/m²) and the exclusion of any plete abstinence from food was required for
pre-existing conditions such as metabolic disorders, serious ill- 2 days of the week. The fasting days had to
nesses, and psychiatric conditions including eating disorders. The be non-consecutive – they had to be separa-
exclusion criteria were defined as regular use of medication (with ted by at least one non-fasting day. One im-
the exception of contraceptives), pregnancy or breastfeeding, in- portant aspect was that the subjects were not
adequate health condition, special diets (vegan, low-carb, ketoge- allowed to eat anything after 8:00 p.m. on
nic), and excessive consumption of nicotine or alcohol. the day before a fasting day. In addition, the
Out of 41 potential subjects, 19 were able to be recruited for the subjects were instructed to refrain from exces-
study. Out of the 19 subjects who were enrolled, 13 completed sive exercise on the day before a fasting day
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(e.g. jogging for longer than 30 minutes). On EBISpro 2016 nutrition software. The daily energy requirement
the fasting days, unrestricted consumption was calculated based on a PAL (physical activity level) of 1.6.
of unsweetened tea, water, and broth was al-
lowed. Food intake was deliberately left unres- Capillary blood measurement
tricted on the non-fasting days so that natural The Freestyle Precision Neo from Abbott (Witney, Oxon/UK) was
behavior after a day of strict fasting could be used as the device for capillary blood measurement, along with
documented. the corresponding test strips for β-ketones and glucose (Abbott;
A 24-hour recall was carried out on the day Witney, Oxon/UK). Alcohol swabs were provided for pre-cleaning
after food intake to record the previous day’s of the skin area.
consumption. This was done either face-to-
face or through an online interview via web- Statistical evaluation
cam. Self-measurement of the blood para- Prior to the study, a sample size calculation was performed based
meters (βHB, glucose) was carried out in the on the primary target parameter of βHB in the blood (μ1 = 0.2;
morning after getting up and in the evening μ2 = 0.5; β = 0.05; power = 0.9) using the GPower 3.1 program.
before going to bed. Alcoholic beverages were The power analysis showed that the required sample size was 14
to be avoided for the entire intervention week. study subjects. In order to ensure statistical validity, the sample
For practical reasons, the total study popula- size was increased by 20% (expected drop-out rate) to 17 subjects.
tion was randomized into two groups (doub- The statistical analysis was carried out using IBM SPSS Statistics
le-blind), with no differences in study conduct. 24 and Microsoft Excel 2016. In addition to descriptive statistical
• Figure 1 shows the course of the study. methods such as mean value, median and standard deviation, ad-
ditional statistical inference methods were applied. Normal distri-
24-hour dietary recall (24HR) bution was checked for using histogram analysis and established
The 24HR records the subjects’ consumption statistical tests (Shapiro-Wilk test, Kolmogorov-Smirnov test).
within the last 24 hours through targeted, In the case of normal distribution, the t-test was used for com-
repeated questions by the interviewer. The in- bined samples; in the case of non-normally distributed samples,
terviewers were all nutrition specialists (BSc the Wilcoxon signed-rank test was used to determine statistically
or MSc in home and nutrition sciences). After significant differences.
the nutrition specialists had been given in-
depth training, the interview was conducted
in a standardized manner using a template
(SOP). The protocols were evaluated using the
study phase
preparation/
intervention final discussion
group allocation
timings
4 days prior to intervention duration: 7 days (2 days fasting,
1 day after the intervention
(duration: 2 h) 5 days normal eating)
data collection
body weight β-hydroxybutyrate (2 x/day) body weight
height blood glucose (2 x/day)
24-hour recall (5 x/week)
Fig. 1: Diagram showing the course of the study with details of the phases, duration, and type of data collection
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Results in the blood in the evening was 1.22 ± 0.74
mmol/L (min./max. = 0.4/2.9 mmol/L), and
Duration of fasting and side effects on the following morning it was 2.58 ± 1.34
The duration of fasting on the two days of fasting was between mmol/L (min./max. = 0.4/4.3 mmol/L).
32 and 41.5 hours (37 ± 2.1 h), depending on the personal rou- The following fasting day, fasting day 2 (F2)
tine of the subjects. In one case, fasting was stopped early on the showed significantly lower βHB values com-
second day of fasting due to feeling unwell. pared to F1 in the evening measurement (0.77
After the first day of fasting, 7 subjects reported mild to moderate ± 0.33; min./max. = 0.2/1.4 mmol/L), and
side effects such as dizziness, shaking, tachycardia, headache, and in the measurement on the following morning
nausea. The symptoms mostly occurred at night and on the mor- (1.14 ± 0.82; min./max. = 0.6/3.5 mmol/L).
ning after the fasting day. In addition, a strong feeling of hunger All measured increases in βHB on F1 and F2
was more frequently reported on the first fasting day. were at a significant level in comparison to the
On the second fasting day, the subjects were already finding it morning fasting value (• Figure 2). Further
easier to abstain from food, and the previously described physical significant differences were found in the eve-
symptoms did not reappear, except in one case. Three of the sub- ning measurement (p = 0.021) and the next
jects experienced no problems during fasting days. morning measurement (p = 0.004) between
the fasting days.
βHB measurement
The βHB values after overnight fasting were on average 0.14 ± Glucose measurement
0.08 mmol/L on non-fasting days (NF), and 0.12 ± 0.09 mmol/L At the start of the fasting day, average blood
on fasting days (F; p = 0.195). glucose values of 85.0 ± 6.3 mg/dL were re-
With the exception of the morning measurement, there were con- corded. As with the measurement of ketone
siderable differences between the measured values on the indivi- bodies, there was a difference between F1 and
dual fasting days. On fasting day 1 (F1) the βHB concentration F2. In the evening of F1 (74.0 ± 7.2 mg/dL)
p=0.004
p=0.021
4.5
4.0
3.5
3.0
2.5
2.0
1.5
1.0
0.5
0.0
F1 morning F1 evening F1 following morning F2 morning F2 evening F2 following morning
Fig. 2: Average βHB concentrations (mmol/L) on the two fasting days (F1, F2) in the morning, in the evening, and on
the morning after fasting
▫ F1 morning vs. F1 evening, p # 0.001
◊ F1 morning vs. F1 following morning, p # 0.001
• F2 morning vs. F2 evening, p # 0.001
∆ F2 morning vs. F2 following morning, p # 0.001
βHB = β-hydroxybutyrate
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p=0.015
glucose (mg/dL)
F1 morning F1 evening F1 following morning F2 morning F2 evening F2 following morning
Fig. 3: Average blood glucose concentrations (mmol/L) on the two fasting days (F1, F2) in the morning, in the
evening, and on the morning after fasting
▫ F1 morning vs. F1 evening, p = 0.001
◊ F1 morning vs. F1 following morning, p # 0.001
• F2 morning vs. F2 evening, p = 0.013
∆ F2 morning vs. F2 following morning, p = 0.001
the glucose concentration was slightly lower take of nutrients on the eating days, which was neither particu-
than on F2 (77 ± 9.6 mg/dL; p = 0.235). A larly low nor particularly high in carbohydrates or fat.
significantly larger difference between F1 (59.0
± 4.7 mg/dL) and F2 (69.0 ± 10.4 mg/dL; p =
0.015) was found the morning after the respec-
tive fasting day. A comparison of the morning Discussion
measurement with the measurements from the
evening and the following morning showed a The reported side effects occurred more frequently in the mor-
significant reduction in blood glucose concent- ning after F1, but either did not occur, or were very mild after
ration on both fasting days (• Figure 3). F2. The blood glucose levels were significantly higher on F2 than
on F1, but were still slightly lower than the values measured at
Body weight and energy intake the beginning of fasting (F1 in the morning, F2 in the morning).
The calculated average energy requirement per The reduced side effects could therefore be a result of the higher
day was 2,277 ± 76 kcal and actual intake average blood glucose concentration, or a result of habituation.
was on average ~ 225 kcal (2,052 ± 312 kcal; It is known from the diabetes research that patients adapt to hy-
p = 0.04) lower. The result was a weight loss poglycemia [23, 24]. Furthermore, it was found that reactions to
of -0.8 ± 0.9 kg (p = 0.013) among the sub- low blood glucose levels varied widely among individual subjects,
jects during the 7-day intervention phase. In which indicates that tolerance differs from person to person. One
two cases, excess energy intake and an accom- way to reduce side effects is to follow a 16:8 diet. However, this
panying weight gain (of 0.2 and 1.5 kg res- very likely leads to significantly lower ketone body values in the
pectively) was observed. Based on the 24HR, blood, in line with the measured value determined in this study
there was no strong increase in food intake after nightly fasting (~ 0.2 mmol/L). A further option is the use
after the fasting days. The overall evaluation of the 5:2 Diet with 25% of normal energy intake being permitted
of the 24-hour recalls showed a balanced in- on a fasting day.
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The measured βHB values for overnight-fas- This paper does not provide the exact values [6]. Antoni et al.
ting of 0.12 ± 0.09 mmol/L correspond to found βHB values of 0.56 ± 0.11 mmol/L in healthy, overweight
the values known in the literature, which or obese subjects after one day of complete energy restriction.
vary between 0.07 and 0.27 mmol/L, depen- Repeating the fasting state was not planned as part of the overall
ding on the study subjects selected [25, 26]. In intervention [30]. A comparison of the results obtained showed
addition to gender, weight, and especially the a considerable difference, which could have been caused by the
presence of metabolic diseases such as diabetes differences in weight (BMI < 25 vs. BMI > 25), age, nutritional
also play a role [15, 25]. These influences were behavior or differences in compliance. Further studies are required
greatly reduced through the targeted, uniform to better understand the effects on the formation of ketone bodies
selection of the exclusively female study po- in different groups.
pulation.
Weight loss was not planned as part of the scope of the inter-
Based on the premise that the physical condi- vention. The weight loss that occurred may have been due to the
tion of ketosis is present starting from a mea- depletion of glycogen stores and the associated water loss and/
sured value of > 2 mmol/L, the data obtained or due to the energy deficit that was measured [15, 31, 32]. Due
shows that ketosis can be achieved at the start to the short intervention period of this study and its different
of the 5:2 diet (F1) in particular [27]. On the focus, no statement can be made regarding the long-term effects
following fasting day (F2), such high values of intermittent fasting on body weight. Studies with longer inter-
were observed only in isolated cases. The dif- vention periods and a primary focus on body weight indicate that
ferences in βHB levels between individuals are continued weight loss takes place [3–6, 9, 19].
known in the literature and they amount to
approximately 30–50% [25, 28]. In the pre-
sent study, deviations of 40–60% of the stan- Limitations
dard deviation were found. The drop-out rate was 32% – markedly higher than the estimated
rate of 20% that was calculated before the study. This effect is
mainly attributable to the time of year in which the study took
Based on the data, it can be con- place (winter) and the limitations associated with this, such as the
cluded that even short-term in- occurrence of colds. An additional factor is the lack of time that
termittent fasting can lead to an many people experience in the run-up to Christmas, which can
increase in ketogenesis, and even lead to discontinuation of study participation, especially when
to the attainment of ketosis. there is no financial incentive.
Given the very large difference between the values, the shortfall in
It is interesting that there is a significant diffe- the sample size should be viewed as a non-critical limitation of the
rence in βHB values between F1 and F2 – this study. Due to the conservative calculation of the sample size, the
points to rapid metabolic adaptation. Accor- expected results were exceeded. The calculated power (0.99) based
ding to the literature, a βHB concentration of on the measured values obtained exceeds the target and ensures
2–3 mmol/L is reached after 24–36 h [15]. the validity of the inductive statistical analysis.
The value on F2 falls far short of this. The
reduced βHB concentration is associated with The potential for factors that influence ketogenesis (such as a high-
a simultaneous increase in blood glucose on fat, low-carbohydrate diet or extensive exercise) to confound the
F2. The increase in blood glucose concentra- results was minimized through the inclusion criteria and the ins-
tion can lead to reduced production of ketone tructions given regarding physical activity during the study [33,
bodies, which explains the observation [29]. In 34]. The uniformly female study population additionally reduced
order to better assess this effect, further stu- the confounding effect of gender differences (some studies report a
dies on intermittent fasting and its impact on higher rate of ketone body release in women) [32, 35, 36].
ketone body production are required.
In existing studies on intermittent fasting, The 24HR method is not free of possible sources of error, so over-
there are hardly any mentions of the forma- reporting and underreporting by the participants is possible. Un-
tion of ketone bodies [3–6, 9, 19]. Harvie et al. dereating and overeating are also known ways in which results
(2013) stated that in the groups that under- may be confounded in this context. The deviation is in line with
went intermittent fasting, there was a slight perceived desired behavior and mostly corresponds to the percei-
increase in the occurrence of short-term eleva- ved expectations of the investigator.
tion of βHB levels in the blood after two days The nutrient database itself is a further potential source of error
of fasting (max. 600 kcal per fasting day). because it may contain incorrect or incomplete data [37].
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